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Ca2+-independent but voltage-dependent secretion in mammalian dorsal root ganglion neurons

Nature Neuroscience volume 5, pages 425–430 (2002)Cite this article

Abstract

We have investigated the Ca2+ dependence of vesicular secretion from the soma of dorsal root ganglion (DRG) neurons, which secrete neuropeptides by exocytosis of dense-core vesicles. In patch-clamped somata of rat DRG neurons, we found a depolarization-induced membrane capacitance increase (ΔCm) in the absence of extracellular Ca2+ and in the presence of a Ca2+ chelator (BAPTA) in the intracellular solution. Depletion of internal Ca2+ stores by thapsigargin in the Ca2+-free bath also did not block the ΔCm, indicating that Ca2+ release from internal Ca2+ stores may not have been involved. Furthermore, the Ca2+-independent ΔCm was blocked by whole-cell dialysis with tetanus toxin and was accompanied by pulsatile secretion of false transmitters, as detected by amperometric measurements. These results indicate the existence of Ca2+-independent but voltage-dependent vesicular secretion (CIVDS) in a mammalian sensory neuron.

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Figure 1: Depolarization-induced capacitance changes in DRG and adrenal chromaffin cells in Ca2+-containing and Ca2+-free baths.
Figure 2: Depolarization-induced ΔCm in the absence of Ca2+ influx in DRG cells.
Figure 3: Combined Cm and [Ca2+]i measurements showed that depolarization induced a ΔCm without a detectable change in [Ca2+]i.
Figure 4: Intracellular Ca2+ microdomains were not involved in depolarization-induced Ca2+-independent ΔCm.
Figure 5: Tetanus toxin (TeNT) blocked depolarization-induced ΔCm in a Ca2+-free bath.
Figure 6: Amperometric detection of depolarization-induced quantal release of false transmitter in a Ca2+-free bath.
Figure 7: Properties of CIVDS.
Figure 8: Comparison of two components of voltage-dependent secretion, CDS and CIVDS, in the same DRG neurons.

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Acknowledgements

We thank L.C. Wang and W. Xiong for cell preparations and help with some experiments; Z.D. You for CGRP radioimmunoassay; T. Xu for advice and the gift of TeNT; and M.M. Poo, E. Neher, R.H. Chow and Y.Z. Wang for helpful comments on the manuscript. This work was supported by grants from Major State Basic Research Program of P.R. China (G2000077800), National Natural Science Foundation of China (39525009, 39970238, 39970371), Chinese Academy of Sciences and The Li Foundation (San Francisco).

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  1. Institute of Neuroscience, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, 320 Yue-Yang Road, Shanghai, 200031, China

    Chen Zhang & Zhuan Zhou

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Correspondence to Zhuan Zhou.

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Zhang, C., Zhou, Z. Ca2+-independent but voltage-dependent secretion in mammalian dorsal root ganglion neurons. Nat Neurosci 5, 425–430 (2002). https://doi.org/10.1038/nn845

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